Antonio Damasio’s notion of “core consciousness” suffers from serious defects. It cannot account for phenomena such as dreaming or locked-in-syndrome, which a proper theory of consciousness should explain, because it requires that the organism’s self-representation be affected by the organism’s processing of an object. This requirement cannot be met in those two states. Moreover, in many states in which the organism does take into account the effect of, say, the perception of an external object, that account is unconscious. And lastly, the close connection Damasio makes between consciousness and the self leads to a theoretically untenable division of the self: evolutionary considerations demand that even a primitive self (e.g., a proto-self) exhibit features of an “autobiographical self”.

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1Antonio Damasio has made so many important contributions to neuroscience that undertaking any criticism of his views must be accompanied by a good amount of trepidation. Nevertheless, it seems to me that the close connections he forges between consciousness and the self result in an unworkable theory of consciousness and are detrimental to his otherwise valuable insistence on providing a biological foundation to our conception of the self.

2My concern is, in particular, Damasio’s division of consciousness into core consciousness and extended consciousness, with the first being a requirement for the presence of the second [Damasio 1999, 82-233], [Damasio & Meyer 2009, 5]. He then ties core consciousness to what he calls the “core self”, the most primitive form of self, which, to preserve the symmetry of his connections, must be considered separate and independent of his “autobiographical self”, in which extended consciousness plays an essential part [Damasio 1999, 100, 156], [Damasio & Meyer 2009, 6-11]. Damasio actually has a two-stage process: proto-self and core self [Damasio 2010, 22-23], but for brevity’s sake I will not address that distinction in this essay. I will argue that “core consciousness” suffers from serious defects. It cannot account for phenomena such as dreaming or locked-in-syndrome, which a proper theory of consciousness should explain, because it requires that the organism’s self representation be affected by the organism’s processing of an object. This requirement cannot be met in those two states. Moreover, in many states in which the organism does take into account the effect of, say, the perception of an external object, that account is unconscious. Another serious problem is that the close connection Damasio makes between consciousness and the self leads to a theoretically untenable division of the self in that (1) evolutionary considerations demand that even a primitive self (i.e., proto-self) exhibit features of an “autobiographical self”, and (2) the self cannot be a conscious self, for the most part.

3In a recently published paper, aptly titled “Consciousness: An overview of the phenomenon and of its possible neural basis”, written with Kaspar Meyer, Damasio tries to cash his key ideas in terms of the latest theoretical and experimental research in neuroscience [Damasio & Meyer 2009]. I will concentrate on that article, with occasional references to some of his significantprevious work.

4In summary, Damasio’s view is as follows. The study of consciousness (actually he speaks of “definition”) can be approached from the observer’s perspective through a combination of behavioral criteria such as wakefulness, background emotions, attention and purposeful behavior [Damasio & Meyer 2009, 4]. The crucial perspective, though, is that of the subject. And Damasio’s main concern is to explain in neural terms how consciousness emerges. From the subject’s perspective, he argues, consciousness emerges when the brain generates:

Neural patterns about objects in sensorimotor terms (images).

Neural patterns about the changes those objects cause in the internal state of the organism; and

A second-order account that interrelates (a) and (b).

5This second-order account describing the relationship between the organism and the object is the neural basis of subjectivity, for it portrays the organism as the protagonist to which objects are referred. In doing so it establishes core consciousness. Now, extended consciousness occurs when objects are related to the organism not only in the “here and now” but in a broader context encompassing “the organism’s past and its anticipated future”. We can think, then, of core consciousness as temporary (“here and now”), whereas extended consciousness uses the resources of working memory and long-term memory.

6Let us see how the self fits this scheme. The production of images (Step (a)) is not enough for consciousness. Consciousness requires something beyond that: it also requires “the creation of a sense of self in the act of knowing”. It creates “knowledge to the effect that we have a mind and that the contents of our mind are shaped in a particular perspective, namely that of our own organism”. Moreover, the “sense of the organism in the act of knowing endows us with the feeling of ownership of the objects to be known” [Damasio & Meyer 2009, 5]. A human organism is said to be conscious when “the representation of objects and events is accompanied by the sense that the organism is the perceiving agent” [Damasio & Meyer 2009, 6]. Damasio & Meyer define consciousness as

a momentary creation of neural patterns which describe a relation between the organism, on the one hand, and an object or event on the other. This composite of neural patterns describe a state that, for lack of a better word, we call the self. That state is the key to subjectivity. [Damasio & Meyer 2009, 6, italics in the original]

7Core consciousness, thus, “provides the organism with a sense of self about one moment, now, and about one place, here” [Damasio & Meyer 2009, 6]. As for this fleeting self, Damasio has unsurprisingly dubbed it “core self” since as early as 1999, in his famous The Feeling of What Happens[Damasio 1999]. Alert readers may have noticed with some alarm my conflation of the self and the sense of self, which they may find unjustified even if I am simply following Damasio’s lead here. In this they are correct, a point I will address after some further exposition of Damasio’s view and some preliminary comments.

8Whereas, core consciousness is “a simple biological phenomenon” that is not dependent on “conventional memory, working memory, reasoning or language”, extended consciousness is complex, depends on memory and is “enhanced by language”. Likewise, the core self is “a transient form of knowledge”, but this is at odds with the traditional notion of self, which is associated with “the idea of identity and personhood”. This traditional notion, according to Damasio & Meyer, corresponds to extended consciousness: “The self that emerges in extended consciousness”, they say, “is a relatively stable collection of the unique facts that characterize a person, the ‘autobiographical self’ ” [Damasio & Meyer 2009, 6]. Keeping track of those unique facts, of course, will depend on semantic memories to some extent, but principally on episodic memories.

9It is crucial for Damasio & Meyer to express Steps (a)–(c) of their hypothesis about the emergence of consciousness in terms of structures of the nervous system. Step (a), the formation of images of objects (including recall in memory), is rather straightforward, given the great progress made by the neuroscience of sensation and perception, even if much still needs to be done. As for Step (b), it is fair to say that Damasio himself has done more than any other person in the field to bring to our attention the importance of accounting for the neural patterns of the changes caused in the representation of the organism by the objects of Step (a) [Damasio 1994, 1999]. Images are then to be appraised in the context of the representation of the body in neural maps in such structures as the brainstem, hypothalamus, insular cortex, cingulate cortex and parietal cortex that allow the organism to keep track of the “state of the internal milieu, the viscera, the vestibular apparatus, and the musculoskeletal system [...] as a set of activities we call the ‘proto-self’ ” [Damasio & Meyer 2009, 8]. Earlier Damasio had defined the proto-self as

a coherent collection of neural patterns which map, moment by moment, the state of the physical structure of the organism in its many dimensions. [Damasio 1999, 154, emphasis in the original]

10The beginning of consciousness is presumably marked by a “non-verbal account” that “describes the relationship” between the “reactive” changes in the proto-self and “the object that causes those changes”, i.e., the relation between Steps (a) and (b) above. Such a non-verbal account “is generated by structures capable of receiving signals from maps that represent both the organism and the object” [Damasio & Meyer 2009, 8]—structures that should, then, prove crucial to the generation of both core and extended consciousness. Damasio’s main candidate all along [Damasio 1994] has been the posteromedial cortex (PMC), which is “the conjunction of the posterior cingulate cortex, the retrosplenial cortex and the precuneus (Brodmann areas 23a/b, 29, 30, 31, 7m)”. The PMC is ideally suited because it has connections, largely reciprocal, “to most all cortical regions [...] and to numerous thalamic nuclei” [Damasio & Meyer 2009, 9], which is important because the generation of all these “second order” neural patterns should involve not only the cortex but also “thalamocortical interactions”. Such richness of connections is quite convenient for it allows for the involvement of working memory and long-term memory, both essential for the development of the autobiographical self. The precuneus, part of the PMC, is activated during the “retrieval of autobiographical events”; the PMC forms part of the resting network, which some researchers have connected to processes concerning the self; and in several brain-imaging studies, the PMC has been activated in tasks “involving reflection on the subjects own personality traits” [Damasio & Meyer 2009, 9]. Furthermore,

all states in which core consciousness is compromised [...] share an important characteristic: they typically have damage and/or altered metabolism in a number of midline structures such as the PMC. [Damasio & Meyer 2009, 10]

11It should be mentioned here that the PMC is not the top choice of most neuroscientists researching the self; many show a marked preference for the medial prefrontal cortex, for example, citing also richness of cortical and thalamic connections, direct involvement of working memory, and most of the rest [Macrae, Heatherton et al. 2004]. Nevertheless, Damasio & Meyer can accommodate the PMC as being a part of a larger network of midline structures.

12Let me begin by pointing out an ambiguity in results from brain imaging studies that are expressed, as cited above in pronouncements about the activation of the PMC (or other structures), in tasks “involving reflection on the subjects own personality traits”. Such tasks are nearly always relative or in contrast to other tasks. As an example consider an fMRI self-attribution study I performed with my colleague Matthew Cole in Mark Haacke’s MR Lab at Harper’s Hospital of Wayne State University. We asked subjects to answer questions about personality traits concerning themselves and their best friends (e.g., “Are you kind?”, “Is your best friend kind?”). In another condition we also asked whether they would attribute to themselves or their best friends several non-personality traits (e.g., “Are you tall?”, “Is your best friend tall?). In the contrast between the combined Self conditions versus the combined Best Friend conditions, as can be seen in Figure 1, self-attribution showed a marked differential activation of Brodmann area 31, part of the PMC, in this particular contrast. Thus it seems at first that my own experimental work supports Damasio’s theoretical argument.

Figure 1: Significant activation of the Limbic Lobe, and the Cingulate Gyrus in Brodmann Area 31 (Self — Best Friend). Composite average picture of 13 participants. fMRI study on the neural correlates of the self. G. Munévar & M. Cole.

13Nevertheless, when the contrast of combined conditions was between Self and a celebrity the participants did not know personally (Bill Gates), the results were quite different; that is, a completely different region, the anterior cingulate cortex (ACC), was shown to have the greatest differential activation, as can be seen in Figure 2. This result, obtained with exactly the same participants in the very same sessions in the fMRI scanner, no longer seems to support Damasio’s theoretical argument (the ACC is not a part of the PMC).

14Unless we take a different approach, the confusion seems to mount when we compare the combined conditions for Best Friend and Bill Gates. As we can see in Figure 3, the pattern of activation is pretty much the same as when comparing the Self and Bill Gates conditions, although the level of activation is smaller.

15Matters become even worse when we vary the tasks. That is, if we do an experiment involving self-recognition instead of self-attribution, as for example asking subjects to identify photographs of themselves as opposed to those of their best friends or strangers, the areas differentially activated would be completely different [Platek, Loughead et al. 2006]. The proliferation of diverse results may be such as to drive some observers to despair of the neuroscience of the self as a field of research [Northoff, Heinzel et al. 2006]. It seems that there can be many kinds of distinctions between self and others, and many different ways in which the brain can handle such distinctions. As I will briefly discuss below, however, this situation is perfectly consistent with a principled evolutionary explanation of the self, one that, unlike Damasio’s, does not subordinate the self to consciousness.

16Before that discussion, however, it pays to realize that there are other conflicts between Damasio’s view and some important considerations drawn from neuroscience. First, since the autobiographical self as posited by Damasio depends on episodic memories of the subject’s experiences, it is unlikely to be more than an imaginative construct. As Stanley Klein has clearly demonstrated using case studies, the self cannot be constituted by episodic memories, for the very simple reason that patients who are completely unable to form episodic memories (because they no longer have a hippocampus) are nevertheless able to give a reliable account of their personality traits [Klein 2004]. Patients who exhibited serious personality changes after being injured were still able to account for their new personality traits, in spite of having lost the ability to form episodic memories.

17Second, and in keeping with the theme of imaginative constructs, it seems strange that the author of Descartes’ Error should endeavor to subordinate the self to consciousness [Damasio 1994]. This Cartesian commitment stems from Damasio’s goal of explaining the notion of subjectivity, and particularly of why our experiences indeed feel “ours”. But attention to the matter, even at the level of phenomenology, reveals that while undergoing intense perceptual experiences (e.g., listening to music we find truly beautiful) we may enter into a state in which we do not think about ourselves. Francis Crick & Cristopher Koch faced this counterevidence by suggesting that the brain still tags all experiences, although in these cases does so subconsciously, most likely through activation of the frontal areas (even if Damasio’s favored PMC were the key region, it might have to work through the frontal areas, given the lack of connection of the PMC with the primary sensory and motor areas) [Crick & Koch 2003]. But a recent experiment has shown that during intense perceptual tasks the activation of the frontal lobe actually decreases! [Goldberg, Harel et al. 2006].

18Moreover, by conflating the self and the sense of self, as mentioned earlier, Damasio creates serious doubts about the existence of the self. Given his view, it seems fair to suppose that the self is equivalent to an internal perception. Rodolfo Llinas certainly interpreted matters this way. But if so, Llinas concluded, the self is an illusion [Llinas 2001]! Others would speak of a construction instead, still leaving the ontological status of the self up in the air, so to speak. In any event, if we do have a self, whatever it is should be ontologically different from our internal perception of it, just as an elephant surely is ontologically different from our perception of it.

19In any event, Damasio’s insistence on a conscious self runs into other problems. For example, the conscious self as a decision maker clashes with experiments such as those by Libet, in which it was shown that, in flexing a hand, the brain’s unconscious readiness potential takes place 350 milliseconds, on the average, before the subject has the conscious thought of moving thehand [Libet 1985].

20Besides, the effects of the perception on the organism, even when all of Damasio’s requirements for core consciousness are met, are normally worked out unconsciously. We meet a new person and the almost instant non-verbal “processing” of the information depends on a great many clues that themselves depend on unconscious processes based on evolutionary reasons or on a long history of personal experiences. This new person seems trustworthy, interesting, etc., but we often have no idea why the actual conscious experience is connected to these reactions, and we might not even be aware of the reactions themselves. Indeed, as Crick pointed out, most of the brain’s functions, including cognitive functions, are unconscious. We should thus expect that the self, if it exists, is mostly unconscious. When we ignore this point and think of the self as a conscious (or worse, Cartesian) self, then all sorts of paradoxes arise, as we have seen.

21In previous work I proposed that we think about the self in the context of evolutionary biology [Munévar 2008;2012]. Any organism needs to demarcate self from other, but in more complex organisms, such as mammals, meeting that need goes beyond the responses of the immune system, for it requires the coordination of external information with information about the internal states of the organism. Such coordination, to be useful, must take into account the previous experience of the organism, as well as its genetic inheritance in the form, for example, of basic emotions that will guide it to survive, reproduce, etc., as Damasio himself has so skillfully argued. And as he pointed out, experience must be interpreted on the basis of what the organism takes itself to be, but this is, once again, a mostly subconscious task assigned mainly to the central nervous system and particularly to the brain.

22A brain that fails to make the connections necessary to carry out this coordinating and interpreting task puts the organism at a disadvantage. It might, for instance, have difficulty learning or remembering crucial facts about its environment, or it might not be able to disambiguate key perceptual information. A rat’s limbic system, mostly the amygdala and the insula, keeps it from eating food that has made it sick before. This is an unconscious process that has counterparts in human beings as well.

23A brain that has evolved to unify external and internal information in the context of its own history (or rather its representations of it), as well as to distinguish the organism from others, is a brain evolved to carry out the functions normally ascribed to a self: being a self is to a large extent what a brain does. But the brain does it unconsciously (or subconsciously) for the most part. It seems that, given that the brain is distributive, and given the myriad of ways in which the individual needs to be distinguished from others, the self is likely to be distributive as well. That would explain why different “self” tasks in a variety of brain-imaging experiments yield such a variety of patterns of brain activation. And since we are social animals, the evolutionary account also explains why, in the self-attribution experiment used for purposes of illustration above, the contrasts Self–Bill Gates and Best Friend–Bill Gates both activated the ACC (although at different intensities). We tend to identify with those who are close to us. As for the activation of Brodmann Area 31 in the contrast Self–Best Friend: this is the area that underpins the organism’s orientation in terms of “objective” features such as landmarks [Baumann & Mattingley 2010], as opposed to an egocentric orientation (the suggestion is for an “objectification” of the distinction between the organism and those close to it). Orientation is crucial to organisms evolved for action. Incidentally, the activation of the ACC shown in Figures 2 and 3 offers a biological bonus all its own: that area is anatomically diminished in schizophrenics, who are notorious for their difficulties in telling self from others [Fornito, Yücel et al. 2009].

24The question of consciousness will, of course, remain very significant, and Damasio’s account, amended to explain only how consciousness may arise from some changes made by objects to the proto-self, may still bear some fruit. Some puzzles remain, though. For example, in typical dreams during REM sleep, unlike in typical visual perceptions, the body does not react much to the content of the dream experience, since the thalamic-cortical areas become to a large extent functionally “disconnected” from the rest of the brain; and to the small extent that it so reacts, the body’s self-representation is not affected by such content consciously. To do so we would have to be aware that we are dreaming, and we generally are not. Some individuals, sometimes, are aware that they are dreaming. Such cases are instances of “lucid dreams”. But most people most of the time do not have lucid dreams.

25In locked-in-syndrome, a patient is conscious even though he is completely paralyzed. Not only are Damasio’s requirements for core consciousness not met, even though the patient should have at least core consciousness, this syndrome is caused by damage to the pons, one of the very structures in the brain that Damasio considers essential for core consciousness.

26None of above is meant to imply that consciousness plays no part in our mental life, or indeed in forming our sense of self. But what that part may be still needs to be elucidated. One interesting hypothesis, already mentioned, is to consider consciousness as akin to an internal perception, and on occasion an internal perception of the self, subject to vagaries and illusions as all other perceptions are. Be that as it may, it seems that Damasio’s forcing of consciousness on the self does not succeed and, instead, detracts from some of his important insights about the mind.

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Figure 1: Significant activation of the Limbic Lobe, and the Cingulate Gyrus in Brodmann Area 31 (Self — Best Friend). Composite average picture of 13 participants. fMRI study on the neural correlates of the self. G. Munévar & M. Cole.